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Effects of Urea Removal on the Stable Isotopes δ13C and δ15N in Rays from the Coastal Waters of Peninsular Malaysia
Corresponding Author(s) : Maizah Mohd Abdullah
Jurnal Ilmiah Perikanan dan Kelautan, Vol. 14 No. 2 (2022): JURNAL ILMIAH PERIKANAN DAN KELAUTAN
Abstract
Highlight Research
- This is the first stable isotopes study of rays from Malaysian waters
- Urea extraction significantly enriched the δ15N values ("°)
- Urea removal is obliged for stable isotope studies on rays
- Such methodological information is critical for marine research in the region
Abstract
This is the first reported record of stable isotope values for elasmobranch rays within Malaysian waters, and serves as an important baseline methodological information for future studies investigating stable isotope values in both shark and ray species in the region. This study examined the effects of urea removal on the stable isotopes values of δ13C and δ15N in muscle tissues sampled from several elasmobranch rays species, namely Pastinachus atrus, Rhinoptera javanica, Himantura gerrardi, Himantura uarnak and Aetobatus ocellatus. Individual ray species were collected in July and August of 2018, from the coastal waters of Terengganu State, Malaysia. Urea removal was performed by soaking muscle tissue samples in deionised water for at least 24 hours before being dehydrated. The resulting stable isotope values of these samples were compared to samples that did not undergo the urea removal process. Stable isotope values were individual and species-specific, however, the effect of urea removal was significant for δ15N values but did not significantly affect the δ13C values. We conclude that removing urea from elasmobranch samples before stable isotope analysis is advisable to draw correct conclusions about the animal's diets.
Keywords
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- Ahmad, A., Lim, A.P.K., Fahmi, Dharmadi & Krajangdara, T. (2014). Field guide to rays, skates, and chimaeras of the Southeast Asian Region. Kuala Lumpur: Perpustakaan Negara Malaysia.
- Bachok, Z., Mansor, M. I., & Noordin, R. M. (2004). Diet composition and food habits of demersal and pelagic marine fishes from Terengganu waters, east coast of Peninsular Malaysia. NAGA, WorldFish Center Quarterly, 27(3-4):41-47.
- Ballantyne, J. S. (1997). Jaws: the inside story. The metabolism of elasmobranch fishes. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 118(4):703-742.
- Berthe, C., Waqalevu, V. P., Latry, L., Besson, M., Lerouvreur, F., Siu, G., Lecellier, G., Rummer, J. L., Bertucci, F., Iglesias, S., & Lecchini, D. (2018). Distribution patterns of ocellated eagle rays, Aetobatus ocellatus, along two sites in Moorea Island, French Polynesia. Cybium, 42(4):313-320.
- Bornatowski, H., Navia, A. F., Braga, R. R., Abilhoa, V., & Corríªa, M. F. M. (2014). Ecological importance of sharks and rays in a structural foodweb analysis in southern Brazil. ICES Journal of Marine Science, 71(7):1586-1592.
- Borrell, A., Cardona, L., Kumarran, R. P., & Aguilar, A. (2011). Trophic ecology of elasmobranchs caught off Gujarat, India, as inferred from stable isotopes. ICES Journal of Marine Science, 68(3):547-554.
- Burgess, K. B., Couturier, L. I., Marshall, A. D., Richardson, A. J., Weeks, S. J., & Bennett, M. B. (2016). Manta birostris, predator of the deep? Insight into the diet of the giant manta ray through stable isotope analysis. Royal Society Open Science, 3(11):160717.
- Burgess, K. B., & Bennett, M. B. (2016). Effects of ethanol storage and lipid and urea extraction on δ15N and δ13C isotope ratios in a benthic elasmobranch, the bluespotted maskray Neotrygon kuhlii. Journal of Fish Biology, 90(1):417-423.
- Carlisle, A. B., Kim, S. L., Semmens, B. X., Madigan, D. J., Jorgensen, S. J., Perle, C. R., & Block, B. A. (2012). Using stable isotope analysis to understand the migration and trophic ecology of Northeastern Pacific white sharks (Carcharodon carcharias). PLoS ONE, 7(2):e30492.
- Chong, V. C., Low, C. B., & Ichikawa, T. (2001). Contribution of mangrove detritus to juvenile prawn nutrition: A dual stable isotope study in a Malaysian mangrove forest. Marine Biology, 138(1):77-86.
- Christensen, D. R., & Moore, B. C. (2009). Using stable isotopes and a multiple-source mixing model to evaluate fish dietary niches in a mesotrophic lake. Lake and Reservoir Management, 25(2):167-175.
- Collins, A. B., Heupel, M. R., Hueter, R. E., & Motta, P. J. (2007). Hard prey specialists or opportunistic generalists? An examination of the diet of the cownose ray, Rhinoptera bonasus. Marine and Freshwater Research, 58(1):135-144.
- Couturier, L. I., Rohner, C. A., Richardson, A. J., Marshall, A. D., Jaine, F. R. A., Bennett, M. B., Townsend, K. A., Weeks, S. J., & Nichols, P. D. (2013). Stable isotope and signature fatty acid analyses suggest reef manta rays feed on demersal zooplankton. PLoS ONE, 8(10):e77152.
- Crook, K. A., Barnett, A., Sheaves, M., & Abrantes, K. (2019). Effects of lipid and urea extraction on stable isotope values (δ13C and δ15N) of two batoids: A call for more species"specific investigations. Limnology and Oceanography: Methods, 17(11):565-574.
- DeNiro, M. J., & Epstein, S. (1978). Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta, 42(5):495-506.
- English, M. D., Robertson, G. J., & Mallory, M. L. (2015). Trace element and stable isotope analysis of fourteen species of marine invertebrates from the Bay of Fundy, Canada. Marine Pollution Bulletin, 101(1):466-472.
- Fisk, A. T., Tittlemier, S. A., Pranschke, J. L., & Norstrom, R. J. (2002). Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of Greenland sharks. Ecology, 83(8):2162-2172.
- Goldstein, L. E. O. N., Oppelt, W. W., & Maren, T. H. (1968). Osmotic regulation and urea metabolism in the lemon shark Negaprion brevirostris. American Journal of Physiology-Legacy Content, 215(6):1493-1497.
- Hussey, N. E., MacNeil, M. A., Olin, J. A., McMeans, B. C., Kinney, M. J., Chapman, D. D., & Fisk, A. T. (2012). Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions. Journal of Fish Biology, 80(5):1449-1484.
- Kim, S. L., & Koch, P. L. (2012). Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis. Environmental Biology of Fishes, 95(1):53-63.
- Last, P. R., White, W. T., De Carvalho, M. R., Séret, B., Stehmann, M. F. W., & Naylor, G. J. P. (2016). Rays of the world. Australia: CSIRO Publishing.
- Li, Y., Zhang, Y., Hussey, N. E., & Dai, X. (2016). Urea and lipid extraction treatment effects on δ15N and δ13C values in pelagic sharks. Rapid Communications in Mass Spectrometry, 30(1):1-8.
- MacNeil, M. A., Skomal, G. B., & Fisk, A. T. (2005). Stable isotopes from multiple tissues reveal diet switching in sharks. Marine Ecology Progress Series, 302:199-206.
- Michael, S. W. (1993). Reef sharks and rays of the world. A guide to their identification, behavior, and ecology. California: Sea Challengers.
- Mohidin, N. A. H. B., Hajisamae, S., Abdullah, M. M., Hashim, M., Habib, A., Islam, R., & Fazrul, H. (2021). Species composition and distribution pattern of stingrays in the coastal waters of Terengganu, Malaysia, the South China Sea. Chiang Mai Journal of Science, 48(4):1009-1020.
- Mukhtar, A., Zulkifli, S. Z., Mohamat-Yusuff, F., & Ismail, A. (2016). Stable isotope (δ13C and δ15N) analysis as a tool to quantify the food web structure in seagrass area of Pulai River estuary, Johor, Peninsular Malaysia. Malayan Nature Journal, 68(1-2):91-102.
- Newell, R. I. E., Marshall, N., Sasekumar, A., & Chong, V. C. (1995). Relative importance of benthic microalgae, phytoplankton, and mangroves as sources of nutrition for penaeid prawns and other coastal invertebrates from Malaysia. Marine Biology, 123(3):595-606.
- Nielsen, J., Christiansen, J. S., Gronkjaer, P., Bushnell, P., Steffensen, J. F., Kiilerich, H. O., Praebel, K., & Hedeholm, R. (2019). Greenland shark (Somniosus microcephalus) stomach contents and stable isotope values reveal an ontogenetic dietary shift. Frontiers in Marine Science, 6:125.
- O'Shea, O. R., Thums, M., Van Keulen, M., Kempster, R. M., & Meekan, M. G. (2013). Dietary partitioning by five sympatric species of stingray (Dasyatidae) on coral reefs. Journal of fish biology, 82(6):1805-1820.
- Pankow, C. J., Macdonald, C. C., Shiffman, D. S., Wester, J., & Abel, D. (2021). Stable isotopic dynamics of juvenile elasmobranchs in a South Carolina nursery area. Southeastern Naturalist, 20(1):92-104.
- Peel, L. R., Daly, R., Keating Daly, C. A., Stevens, G. M., Collin, S. P., & Meekan, M. G. (2019). Stable isotope analyses reveal unique trophic role of reef manta rays (Mobula alfredi) at a remote coral reef. Royal Society open science, 6(9):190599.
- Pillans, R. D., Good, J. P., Anderson, W. G., Hazon, N., & Franklin, C. E. (2005). Freshwater to seawater acclimation of juvenile bull sharks (Carcharhinus leucas): plasma osmolytes and Na+/K+-ATPase activity in gill, rectal gland, kidney and intestine. Journal of Comparative Physiology B, 175(1):37-44.
- Sampson, L., Galván-Magaña, F., De Silva-Dávila, R., Aguíñiga-García, S., & O'Sullivan, J. (2010). Diet and trophic position of the devil rays Mobula thurstoni and Mobula japanica as inferred from stable isotope analysis. Journal of the Marine Biological Association of the United Kingdom, 90(5):969-976.
- Schluessel, V., Bennett, M. B., & Collin, S. P. (2010). Diet and reproduction in the white-spotted eagle ray Aetobatus narinari from Queensland, Australia and the Penghu Islands, Taiwan. Marine and freshwater research, 61(11):1278-1289.
- Wood, C. M., Bucking, C., Fitzpatrick, J., & Nadella, S. (2007). The alkaline tide goes out and the nitrogen stays in after feeding in the dogfish shark, Squalus acanthias. Respiratory physiology & neurobiology, 159(2):163-170.
- Yano, K., Ahmad, A., Gambang, A. C., Idris, A. H., Solahuddin, A. R., & Aznan, Z. (2005). Sharks and rays of Malaysia and Brunei Darussalam. Kuala Terengganu: SEAFDEC/MFRDMD.
- Zulkifli, S. Z., Mohamat-Yusuff, F., Mukhtar, A., Ismail, A., & Miyazaki, N. (2014). Determination of food web in intertidal mudflat of tropical mangrove ecosystem using stable isotope markers: A preliminary study. Life Science Journal, 11(3):427-431.
- Zulkifli, S. Z., Hanapiah, M., Joni, A. A. M., & Mukhtar, A. (2016). Utilisation of dual stable isotopes to determine trophic structure in a mangrove-intertidal mudflat of Johor Strait, Malaysia. Ecology, Environment and Conservation, 22(3):1123-1128.
References
Ahmad, A., Lim, A.P.K., Fahmi, Dharmadi & Krajangdara, T. (2014). Field guide to rays, skates, and chimaeras of the Southeast Asian Region. Kuala Lumpur: Perpustakaan Negara Malaysia.
Bachok, Z., Mansor, M. I., & Noordin, R. M. (2004). Diet composition and food habits of demersal and pelagic marine fishes from Terengganu waters, east coast of Peninsular Malaysia. NAGA, WorldFish Center Quarterly, 27(3-4):41-47.
Ballantyne, J. S. (1997). Jaws: the inside story. The metabolism of elasmobranch fishes. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 118(4):703-742.
Berthe, C., Waqalevu, V. P., Latry, L., Besson, M., Lerouvreur, F., Siu, G., Lecellier, G., Rummer, J. L., Bertucci, F., Iglesias, S., & Lecchini, D. (2018). Distribution patterns of ocellated eagle rays, Aetobatus ocellatus, along two sites in Moorea Island, French Polynesia. Cybium, 42(4):313-320.
Bornatowski, H., Navia, A. F., Braga, R. R., Abilhoa, V., & Corríªa, M. F. M. (2014). Ecological importance of sharks and rays in a structural foodweb analysis in southern Brazil. ICES Journal of Marine Science, 71(7):1586-1592.
Borrell, A., Cardona, L., Kumarran, R. P., & Aguilar, A. (2011). Trophic ecology of elasmobranchs caught off Gujarat, India, as inferred from stable isotopes. ICES Journal of Marine Science, 68(3):547-554.
Burgess, K. B., Couturier, L. I., Marshall, A. D., Richardson, A. J., Weeks, S. J., & Bennett, M. B. (2016). Manta birostris, predator of the deep? Insight into the diet of the giant manta ray through stable isotope analysis. Royal Society Open Science, 3(11):160717.
Burgess, K. B., & Bennett, M. B. (2016). Effects of ethanol storage and lipid and urea extraction on δ15N and δ13C isotope ratios in a benthic elasmobranch, the bluespotted maskray Neotrygon kuhlii. Journal of Fish Biology, 90(1):417-423.
Carlisle, A. B., Kim, S. L., Semmens, B. X., Madigan, D. J., Jorgensen, S. J., Perle, C. R., & Block, B. A. (2012). Using stable isotope analysis to understand the migration and trophic ecology of Northeastern Pacific white sharks (Carcharodon carcharias). PLoS ONE, 7(2):e30492.
Chong, V. C., Low, C. B., & Ichikawa, T. (2001). Contribution of mangrove detritus to juvenile prawn nutrition: A dual stable isotope study in a Malaysian mangrove forest. Marine Biology, 138(1):77-86.
Christensen, D. R., & Moore, B. C. (2009). Using stable isotopes and a multiple-source mixing model to evaluate fish dietary niches in a mesotrophic lake. Lake and Reservoir Management, 25(2):167-175.
Collins, A. B., Heupel, M. R., Hueter, R. E., & Motta, P. J. (2007). Hard prey specialists or opportunistic generalists? An examination of the diet of the cownose ray, Rhinoptera bonasus. Marine and Freshwater Research, 58(1):135-144.
Couturier, L. I., Rohner, C. A., Richardson, A. J., Marshall, A. D., Jaine, F. R. A., Bennett, M. B., Townsend, K. A., Weeks, S. J., & Nichols, P. D. (2013). Stable isotope and signature fatty acid analyses suggest reef manta rays feed on demersal zooplankton. PLoS ONE, 8(10):e77152.
Crook, K. A., Barnett, A., Sheaves, M., & Abrantes, K. (2019). Effects of lipid and urea extraction on stable isotope values (δ13C and δ15N) of two batoids: A call for more species"specific investigations. Limnology and Oceanography: Methods, 17(11):565-574.
DeNiro, M. J., & Epstein, S. (1978). Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta, 42(5):495-506.
English, M. D., Robertson, G. J., & Mallory, M. L. (2015). Trace element and stable isotope analysis of fourteen species of marine invertebrates from the Bay of Fundy, Canada. Marine Pollution Bulletin, 101(1):466-472.
Fisk, A. T., Tittlemier, S. A., Pranschke, J. L., & Norstrom, R. J. (2002). Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of Greenland sharks. Ecology, 83(8):2162-2172.
Goldstein, L. E. O. N., Oppelt, W. W., & Maren, T. H. (1968). Osmotic regulation and urea metabolism in the lemon shark Negaprion brevirostris. American Journal of Physiology-Legacy Content, 215(6):1493-1497.
Hussey, N. E., MacNeil, M. A., Olin, J. A., McMeans, B. C., Kinney, M. J., Chapman, D. D., & Fisk, A. T. (2012). Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions. Journal of Fish Biology, 80(5):1449-1484.
Kim, S. L., & Koch, P. L. (2012). Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis. Environmental Biology of Fishes, 95(1):53-63.
Last, P. R., White, W. T., De Carvalho, M. R., Séret, B., Stehmann, M. F. W., & Naylor, G. J. P. (2016). Rays of the world. Australia: CSIRO Publishing.
Li, Y., Zhang, Y., Hussey, N. E., & Dai, X. (2016). Urea and lipid extraction treatment effects on δ15N and δ13C values in pelagic sharks. Rapid Communications in Mass Spectrometry, 30(1):1-8.
MacNeil, M. A., Skomal, G. B., & Fisk, A. T. (2005). Stable isotopes from multiple tissues reveal diet switching in sharks. Marine Ecology Progress Series, 302:199-206.
Michael, S. W. (1993). Reef sharks and rays of the world. A guide to their identification, behavior, and ecology. California: Sea Challengers.
Mohidin, N. A. H. B., Hajisamae, S., Abdullah, M. M., Hashim, M., Habib, A., Islam, R., & Fazrul, H. (2021). Species composition and distribution pattern of stingrays in the coastal waters of Terengganu, Malaysia, the South China Sea. Chiang Mai Journal of Science, 48(4):1009-1020.
Mukhtar, A., Zulkifli, S. Z., Mohamat-Yusuff, F., & Ismail, A. (2016). Stable isotope (δ13C and δ15N) analysis as a tool to quantify the food web structure in seagrass area of Pulai River estuary, Johor, Peninsular Malaysia. Malayan Nature Journal, 68(1-2):91-102.
Newell, R. I. E., Marshall, N., Sasekumar, A., & Chong, V. C. (1995). Relative importance of benthic microalgae, phytoplankton, and mangroves as sources of nutrition for penaeid prawns and other coastal invertebrates from Malaysia. Marine Biology, 123(3):595-606.
Nielsen, J., Christiansen, J. S., Gronkjaer, P., Bushnell, P., Steffensen, J. F., Kiilerich, H. O., Praebel, K., & Hedeholm, R. (2019). Greenland shark (Somniosus microcephalus) stomach contents and stable isotope values reveal an ontogenetic dietary shift. Frontiers in Marine Science, 6:125.
O'Shea, O. R., Thums, M., Van Keulen, M., Kempster, R. M., & Meekan, M. G. (2013). Dietary partitioning by five sympatric species of stingray (Dasyatidae) on coral reefs. Journal of fish biology, 82(6):1805-1820.
Pankow, C. J., Macdonald, C. C., Shiffman, D. S., Wester, J., & Abel, D. (2021). Stable isotopic dynamics of juvenile elasmobranchs in a South Carolina nursery area. Southeastern Naturalist, 20(1):92-104.
Peel, L. R., Daly, R., Keating Daly, C. A., Stevens, G. M., Collin, S. P., & Meekan, M. G. (2019). Stable isotope analyses reveal unique trophic role of reef manta rays (Mobula alfredi) at a remote coral reef. Royal Society open science, 6(9):190599.
Pillans, R. D., Good, J. P., Anderson, W. G., Hazon, N., & Franklin, C. E. (2005). Freshwater to seawater acclimation of juvenile bull sharks (Carcharhinus leucas): plasma osmolytes and Na+/K+-ATPase activity in gill, rectal gland, kidney and intestine. Journal of Comparative Physiology B, 175(1):37-44.
Sampson, L., Galván-Magaña, F., De Silva-Dávila, R., Aguíñiga-García, S., & O'Sullivan, J. (2010). Diet and trophic position of the devil rays Mobula thurstoni and Mobula japanica as inferred from stable isotope analysis. Journal of the Marine Biological Association of the United Kingdom, 90(5):969-976.
Schluessel, V., Bennett, M. B., & Collin, S. P. (2010). Diet and reproduction in the white-spotted eagle ray Aetobatus narinari from Queensland, Australia and the Penghu Islands, Taiwan. Marine and freshwater research, 61(11):1278-1289.
Wood, C. M., Bucking, C., Fitzpatrick, J., & Nadella, S. (2007). The alkaline tide goes out and the nitrogen stays in after feeding in the dogfish shark, Squalus acanthias. Respiratory physiology & neurobiology, 159(2):163-170.
Yano, K., Ahmad, A., Gambang, A. C., Idris, A. H., Solahuddin, A. R., & Aznan, Z. (2005). Sharks and rays of Malaysia and Brunei Darussalam. Kuala Terengganu: SEAFDEC/MFRDMD.
Zulkifli, S. Z., Mohamat-Yusuff, F., Mukhtar, A., Ismail, A., & Miyazaki, N. (2014). Determination of food web in intertidal mudflat of tropical mangrove ecosystem using stable isotope markers: A preliminary study. Life Science Journal, 11(3):427-431.
Zulkifli, S. Z., Hanapiah, M., Joni, A. A. M., & Mukhtar, A. (2016). Utilisation of dual stable isotopes to determine trophic structure in a mangrove-intertidal mudflat of Johor Strait, Malaysia. Ecology, Environment and Conservation, 22(3):1123-1128.